Aerobic transformation of zinc into metal sulfide by photosynthetic microorganisms

Applied Microbiology and Biotechnology

Volumn 97, Issue 8, 2013, Pages 3613-3623

  Edwards, Chad D ^a   Beatty, Joseph C ^a   Loiselle, Jacqueline B R ^a   Vlassov, Katya A ^a   Lefebvre, Daniel D ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Algae; Cyanobacteria; Heavy metals; Metal transformation; Sulfate assimilation; Zinc sulfide

Indexed keywords

AEROBIC TRANSFORMATIONS; CHLAMYDOMONAS REINHARDTII; CYANOBACTERIA; ELEVATED CONCENTRATIONS; HEAVY METAL CONTAMINATION; PHOTOSYNTHETIC MICROORGANISMS; SERINE ACETYLTRANSFERASE; SULFATE ASSIMILATION;

ALGAE; AMINO ACIDS; BIOREMEDIATION; GALLIUM ALLOYS; HEAVY METALS; METAL IONS; MICROORGANISMS; SEWAGE; SULFUR COMPOUNDS; ZINC; ZINC COMPOUNDS;

ZINC SULFIDE;

BACTERIAL ENZYME; CYSTATHIONINE GAMMA LYASE; CYSTEINE; O ACETYLSERINE(THIOL)LYASE; SERINE ACETYLTRANSFERASE; SULFIDE; SULFITE; UNCLASSIFIED DRUG; ZINC; ZINC SULFIDE;

BIOREMEDIATION; CYANOBACTERIUM; GREEN ALGA; HEAVY METAL; OXIC CONDITIONS; PHOTOSYNTHESIS; SULFIDE; TRANSFORMATION; ZINC;

AEROBIC METABOLISM; ARTICLE; BACTERIAL CELL; BIOSYNTHESIS; BIOTECHNOLOGICAL PRODUCTION; BIOTRANSFORMATION; CHLAMYDOMONAS REINHARDTII; CULTURE MEDIUM; CYANIDIOSCHYZON MEROLAE; CYANOBACTERIUM; ENZYME ACTIVITY; MICROBIAL GROWTH; NONHUMAN; PHOTOSYNTHESIS; RED ALGA; SUPPLEMENTATION; SYNECHOCOCCUS LEOPOLIENSIS; ZINC METABOLISM;

AEROBIOSIS; BIOTRANSFORMATION; CHLAMYDOMONAS REINHARDTII; CULTURE MEDIA; CYSTATHIONINE GAMMA-LYASE; CYSTEINE; ENVIRONMENTAL POLLUTANTS; PHOTOSYNTHESIS; RHODOPHYTA; SULFIDES; SYNECHOCOCCUS; ZINC;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; CYANIDIOSCHYZON; CYANIDIOSCHYZON MEROLAE; CYANOBACTERIA; RHODOPHYTA; SYNECHOCOCCUS ELONGATUS PCC 6301; SYNECHOCOCCUS LEOPOLIENSIS;

EID: 84876689190     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4636-5     Document Type: Article

References (71)

1. Ahmad A, Mukherjee P, Mandal D, Senapati S, Khan MI, Kumar R, Sastry M (2002) Enzyme mediated extracellular synthesis of CdS nanoparticles by the fungus, Fusarium oxysporum. J Am Chem Soc 124:12108-12109
2. Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32:270-277
3. Bai HJ, Zhang ZM, Guo Y, Yang GE (2009) Biosynthesis of cadmium sulfide nanoparticles by photosynthetic bacteria Rhodopseudomonas palustris. Coll Surf B: Biointerfaces 70:142-146
4. +-ATP synthase from various species. biochemical and biophysical research communications. Biochem Biophys Res Commun 201:487-492
5. Behra R, Landwehrjohann R, Vogal L, Wagner B, Sigg L (2002) Copper and zinc content of periphyton from two rivers as a function of dissolved metal concentration. Aquat Sci 64:300-306
6. Chen J, Wu F, Wang W, Zheng C, Lin G, Dong X, He J, Pei Z, Zheng H (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481-4493
7. Chu L, Ebersole J, Kurzban G, Holt S (1997) Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect Immun 65:3231-3238
8. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev of Plant Biol 53:159-182
9. Dominguez M, Gutierrez F, Leon R, Vilchez C, Vega J, Vigara J (2003) Cadmium increases the activity levels of glutamate dehydrogenase and cysteine synthase in Chlamydomonas reinhardtii. Plant Physiol Biochem 41:828-832
10. Dominguez-Solis J, Lopez-Martin M, Ager F, Ynsa M, Romero L, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotech J 2:469-476
11. Gekeler W, Grill E, Winnacker E, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol 150:197-202
12. Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371-382
13. Gross W, Oesterhelt C (1999) Ecophysiological studies on red alga Galdieria sulphuraria isolated from southwest Iceland. Plant Biol 1:694-700
14. Gross W, Kuver J, Tischendorf G, Bouchaala N, Busch W (1998) Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur J Phycol 33:25-31
15. Groudeva VI, Groudev SN, Doycheva AS (2001) Bioremediation of waters contaminated with crude oil and toxic heavy metals. Int J Miner Process 62:293-299
16. Hancock JT, Lisjak M, Teklic T, Wilson ID, Whiteman M (2011) Hydrogen sulphide and signalling in plants. CAB Reviews: Perspectives in Agriculture, Veterinary Science. Nutr Nat Res 6:1-7
17. Hawkesford MJ, DeKok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382-395
18. Holmes JD, Smith PR, Evans-Gowing R, Richardson DJ, Russell DA, Sodeau JR (1995) Energy-dispersive X-ray analysis of the extracellular cadmium sulfide crystallites of Klebsiella aerogenes. Arch Microbiol 163:143-147
19. Hong JS, Rabinowitz JC (1970) Molar extinction coefficient and iron and sulfide content of clostridial ferredoxin. J Biol Chem 245:4982-4987
20. Hrabak E, Chan C, Gribskov M, Harper J, Choi J, Halford N, Kudla J, Luan S, Nimmo H, Sussman M, Thomas M, Walker-Simmons K, Zhu J, Harmon A (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases RID B-3872-2009. Plant Physiol 132:666-680
21. Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167-182
22. Kawashima CG, Noji M, Nakamura M, Ogra Y, Suzuki KT, Saito K (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153-157
23. Kelly DJA, Budd K, Lefebvre DD (2007) Biotransformation of mercury in pH-stat cultures of eukaryotic freshwater algae. Arch Microbiol 187:45-53
24. Kelly D, Budd K, Lefebvre DD (2006) Mercury analysis of acid- and alkaline-reduced biological samples: identification of meta-cinnabar as the major biotransformed compound in algae. Appl Environ Microbiol 72:361-367
25. Kertesz MA (2001) Bacterial transporters for sulfate and organosulfur compounds. Res Microbiol 152:279-290
26. Kimura H (2011) Hydrogen sulfide: its production, release and functions. Amino Acids 41:113-121
27. Kopriva S (2006) Regulation of sulfate assimilation in arabidopsis and beyond. Ann Bot 97:479-495
28. Lefebvre DD, Edwards CD (2010) Decontaminating heavy metals using photosynthetic microbes. In: Shaw V (ed) Emerging environmental technologies, IIth edn. Springer, New York, pp 57-73
29. Lefebvre DD, Kelly D, Budd K (2007) Biotransformation of Hg(II) by cyanobacteria. Appl Environ Microbiol 73:243-249
30. Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637-644
31. Lyons T, Gasch A, Gaither L, Botstein D, Brown P, Eide D (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc Natl Acad Sci U S A 97:7957-7962
32. MacDiarmid C, Gaither L, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845-2855
33. Maret W (2003) Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 133:1460S-1462S
34. Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653-657
35. Melis A, Chen H (2005) Chloroplast sulfate transport in green algae - genes, proteins and effects. Photosynthesis Res 86:299-307
36. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu L, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen C, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral J, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen C, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WCA, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR, Chlamydomonas Annotation JGI, Team A (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions RID A-3530-2008 RID A-1214-2009 RID A-1755-2010 RID C-1537-2010. Science 318:245-251
37. Mikolajczyk M, Awotunde O, Muszynska G, Klessig D, Dobrowolska G (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165-178
38. Miller B, Heuser T, Zimmer W (1999) A Synechococcus leopoliensis SAUG 1402-1 operon harboring the 1-deoxyxylulose 5-phosphate synthase gene and two additional open reading frames is functionally involved in the dimethylallyl diphosphate synthesis. FEBS Lett 460:485-490
39. Moriarty-Craige S, Jones D (2004) Extracellular thiols and thiol/disulfide redox in metabolism. Annu Rev Nutr 24:481-509
40. Mosulen S, Dominguez M, Vigara J, Vilchez C, Guiraum A, Vega J (2003) Metal toxicity in Chlamydomonas reinhardtii: Effect on sulfate and nitrate assimilation. Biomol Eng 20:199-203
41. Murasugi A, Wada C, Hayashi Y (1983) Occurrence of acid-labile sulfide in cadmium-binding peptide 1 from fission yeast. J Biochem 93:661-664
42. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441-454
43. Niknahad H, O'Brien PJ (2008) Mechanism of sulfite cytotoxicity in isolated rat hepatocytes. Chem Biol Interact 174:147-154
44. Ning H, Zhang C, Yao Y, Yu D (2010) Overexpression of a soybean O-acetylserine (thiol) lyase-encoding gene GmOASTL4 in tobacco increases cysteine levels and enhances tolerance to cadmium stress. Biotech Letters 32:557-564
45. Nozaki H, Toda K, Takano H, Kuroiwa T (2001) The second serine acetyltransferase, bacterial-type O-acetylserine (thiol) lyase and eukaryotic-type O-acetylserine (thiol) lyase from the primitive red alga Cyanidioschyzon merolae. J Plant Res 114:291-300
46. 2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol 9:582-588
47. Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1-10
48. Pinto G, Albertano P, Ciniglia C, Cozzolino S, Pollio A, Yoon H, Bhattacharya D (2003) Comparative approaches to the taxonomy of the genus Galdieria merola (Cyanidiales, Rhodophyta). Cryptogam Algol 24:13-32
49. Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res 86:475-489
50. Rabinowitch H, Fridovich I (1985) Growth of Chlorella sorokiniana in the presence of sulfite elevates cell content of superoxide dismutase and imparts resistance towards paraquat. Planta 164:524-528
51. Rabinowitz JC (1978) [30] Analysis of acid-labile sulfide and sulfhydryl groups. In: Anonymous Methods in Enzymology. Academic, pp 275-277
52. Ravina CG, Barroso C, Vega JM, Gotor C (1999) Cysteine biosynthesis in Chlamydomonas reinhardtii. Molecular cloning and regulation of O-acetylserine(thiol)lyase. Eur J Biochem 264:848-853
53. Reese RN, White CA, Winge DR (1992) Cadmium-sulfide crystallites in Cd-(γEC)nG peptide complexes from tomato. Plant Physiol 98:225-229
54. Rennenberg H (1983) Role of O-Acetylserine in hydrogen sulfide emission from pumpkin leaves in response to sulfate. Plant Physiol 73:560-565
55. Rijstenbil JW, Derksen WJ, Gerringa LJA, Poortvliet TCW, Sandee A, van den Berg M, van Drie J, Wijnholds JA (1994) Oxidative stress induced by copper: defense and damage in the marine planktonic diatom Ditylum brightwellii, grown in continuous cultures with high and low zinc levels. Mar Biol 119:583-590
56. Rippka R, Waterbury J, Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100:419-436
57. Robinson N (1989) Algal metallothioneins: secondary metabolites and proteins. J Appl Phycol 1:5-18
58. Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443-2450
59. Scarano G, Morelli E (2003) Properties of phytochelatin-coated CdS nanocrystallites formed in a marine phytoplanktonic alga (Phaeodactylum tricornutum, Bohlin) in response to Cd. Plant Science 165:803-810
60. Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to l-cysteine. Plant Physiol 70:430-436
61. Siegel LM (1965) A direct microdetermination for sulfide. Anal Biochem 11:126-132
62. Smith FW, Hawkesford MJ, Prosser IM, Clarkson DT (1995) Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol Gen Genet 247:709-715
63. Speiser DM, Abrahamson SL, Banuelos G, Ow DW (1992) Brassica juncea produces a phytochelatin-cadmium-sulfide complex. Plant Physiol 99:817-821
64. Stauber J, Florence T (1987) Mechanism of toxicity of ionic copper and copper-complexes to algae. Mar Biol 94:511-519
65. Sueoka N, Chiang KS, Kates JR (1967) Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi I. Isotopic transfer experiments with a strain producing eight zoospores. J Mol Biol 25:47-66
66. Sweeney RY, Mao C, Gao X, Burt JL, Belcher AM, Georgiou G, Iverson BL (2004) Bacterial biosynthesis of cadmium sulfide nanocrystals. Chem Biol 11:1553-1559
67. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, JdA E, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94:11102-11107
68. Tsuji N, Nishikori S, Iwabe O, Shiraki K, Miyasaka H, Takagi M, Hirata K, Miyamoto K (2004) Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120. Biochem Biophys Res Commun 315:751-755
69. Wang CL, Lum AM, Ozuna SC, Clark DS, Keasling JD (2001) Aerobic sulfide production and cadmium precipitation by Escherichia coli expressing the Treponema denticola cysteine desulfhydrase gene. Appl Microbiol Biotechnol 56:425-430
70. Wang C, Maratukulam P, Lum A, Clark D, Keasling J (2000) Metabolic engineering of an aerobic sulfate reduction pathway and its application to precipitation of cadmium on the cell surface. Appl Environ Microbiol 66:4497-4502
71. Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiol 61:184-189